Expression of Wnt and TGF-β pathway components and key adrenal transcription factors in adrenocortical tumors: Association to carcinoma aggressiveness

Pathology Research and Practice

Volumn 209, Issue 8, 2013, Pages 503-509

  Parviainen, Helka ^a,b   Schrade, Anja ^a,b   Kiiveri, Sanne ^a,b   Prunskaite Hyyryläinen, Renata ^c   Haglund, Caj ^d   Vainio, Seppo ^c   Wilson, David B ^e   Arola, Johanna ^d   Heikinheimo, Markku ^a,b,e  

^a UNIVERSITY OF HELSINKI AND HELSINKI UNIVERSITY HOSPITAL   (Finland)

^b BIOMEDICUM HELSINKI   (Finland)

^c UNIVERSITY OF OULU   (Finland)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenoma; Carcinoma; Inhibin; Signaling pathway; Transcription factor

Indexed keywords

BETA CATENIN; INHIBIN A; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; SMAD2 PROTEIN; SMAD3 PROTEIN; STEROIDOGENIC FACTOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 6;

ADRENAL CORTEX CARCINOMA; ADRENAL CORTEX TUMOR; ADULT; AGED; ARTICLE; CANCER PROGNOSIS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INHIBIN ALPHA GENE; MALE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCORING SYSTEM; SIGNAL TRANSDUCTION; TGF BETA SIGNALING PATHWAY; UPREGULATION; WEISS SCORE; WNT SIGNALING PATHWAY;

ADENOMA; CARCINOMA; INHIBIN; SIGNALING PATHWAY; TRANSCRIPTION FACTOR;

ADRENAL CORTEX NEOPLASMS; ADRENOCORTICAL CARCINOMA; ADULT; AGED; BETA CATENIN; CHILD; FEMALE; GATA6 TRANSCRIPTION FACTOR; HUMANS; IMMUNOHISTOCHEMISTRY; INFANT; INHIBINS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-5; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; PROGNOSIS; REGISTRIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SMAD2 PROTEIN; SMAD3 PROTEIN; STEROIDOGENIC FACTOR 1; SURVIVAL ANALYSIS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; TUMOR MARKERS, BIOLOGICAL; WNT PROTEINS; WNT SIGNALING PATHWAY; YOUNG ADULT;

EID: 84881557332     PISSN: 03440338     EISSN: 16180631     Source Type: Journal    
DOI: 10.1016/j.prp.2013.06.002     Document Type: Article

References (34)

1. Almeida M.Q., Soares I.C., Ribeiro T.C., Fragoso M.C., Marins L.V., Wakamatsu A., Ressio R.A., Nishi M.Y., Jorge A.A., Lerario A.M., Alves V.A., Mendonca B.B., Latronico A.C. Steroidogenic factor 1 overexpression and gene amplification are more frequent in adrenocortical tumors from children than from adults. J. Clin. Endocrinol. Metab. 2010, 95:1458-1462.
2. Anttonen M., Parviainen H., Kyronlahti A., Bielinska M., Wilson D.B., Ritvos O., Heikinheimo M. GATA-4 is a granulosa cell factor employed in inhibin-alpha activation by the TGF-beta pathway. J. Mol. Endocrinol. 2006, 36:557-568.
3. Arola J., Liu J., Heikkila P., Ilvesmaki V., Salmenkivi K., Voutilainen R., Kahri A.I. Expression of inhibin alpha in adrenocortical tumours reflects the hormonal status of the neoplasm. J. Endocrinol. 2000, 165:223-229.
4. Bertherat J., Mosnier-Pudar H., Bertagna X. Adrenal incidentalomas. Curr. Opin. Oncol. 2002, 14:58-63.
5. Bielinska M., Parviainen H., Kiiveri S., Heikinheimo M., Wilson D.B. Review paper: origin and molecular pathology of adrenocortical neoplasms. Vet. Pathol. 2009, 46:194-210.
6. Brunt L.M., Moley J.F. Adrenal incidentaloma. World J. Surg. 2001, 25:905-913.
7. Cadigan K.M., Liu Y.I. Wnt signaling: complexity at the surface. J. Cell Sci. 2006, 119:395-402.
8. Gaujoux S., Pinson S., Gimenez-Roqueplo A.P., Amar L., Ragazzon B., Launay P., Meatchi T., Libe R., Bertagna X., Audebourg A., Zucman-Rossi J., Tissier F., Bertherat J. Inactivation of the APC gene is constant in adrenocortical tumors from patients with familial adenomatous polyposis but not frequent in sporadic adrenocortical cancers. Clin. Cancer Res. 2010, 16:5133-5141.
9. Gummow B.M., Winnay J.N., Hammer G.D. Convergence of Wnt signaling and steroidogenic factor-1 (SF-1) on transcription of the rat inhibin alpha gene. J. Biol. Chem. 2003, 278:26572-26579.
10. Heikkila M., Peltoketo H., Leppaluoto J., Ilves M., Vuolteenaho O., Vainio S. Wnt-4 deficiency alters mouse adrenal cortex function, reducing aldosterone production. Endocrinology 2002, 143:4358-4365.
11. Ito M., Park Y., Weck J., Mayo K.E., Jameson J.L. Synergistic activation of the inhibin alpha-promoter by steroidogenic factor-1 and cyclic adenosine 3',5'-monophosphate. Mol. Endocrinol. 2000, 14:66-81.
12. Jimenez P., Saner K., Mayhew B., Rainey W.E. GATA-6 is expressed in the human adrenal and regulates transcription of genes required for adrenal androgen biosynthesis. Endocrinology 2003, 144:4285-4288.
13. Kaivo-Oja N., Bondestam J., Kamarainen M., Koskimies J., Vitt U., Cranfield M., Vuojolainen K., Kallio J.P., Olkkonen V.M., Hayashi M., Moustakas A., Groome N.P., ten Dijke P., Hsueh A.J., Ritvos O. Growth differentiation factor-9 induces Smad2 activation and inhibin B production in cultured human granulosa-luteal cells. J. Clin. Endocrinol. Metab. 2003, 88:755-762.
14. Kiiveri S., Liu J., Arola J., Heikkila P., Kuulasmaa T., Lehtonen E., Voutilainen R., Heikinheimo M. Transcription factors GATA-6, SF-1, and cell proliferation in human adrenocortical tumors. Mol. Cell. Endocrinol. 2005, 233:47-56.
15. Kiiveri S., Liu J., Westerholm-Ormio M., Narita N., Wilson D.B., Voutilainen R., Heikinheimo M. Differential expression of GATA-4 and GATA-6 in fetal and adult mouse and human adrenal tissue. Endocrinology 2002, 143:3136-3143.
16. Kim A.C., Barlaskar F.M., Heaton J.H., Else T., Kelly V.R., Krill K.T., Scheys J.O., Simon D.P., Trovato A., Yang W.H., Hammer G.D. In search of adrenocortical stem and progenitor cells. Endocr. Rev. 2009, 30:241-263.
17. Kuulasmaa T., Jaaskelainen J., Suppola S., Pietilainen T., Heikkila P., Aaltomaa S., Kosma V.M., Voutilainen R. WNT-4 mRNA expression in human adrenocortical tumors and cultured adrenal cells. Horm. Metab. Res. 2008, 40:668-673.
18. Lefrancois-Martinez A.M., Bertherat J., Val P., Tournaire C., Gallo-Payet N., Hyndman D., Veyssiere G., Bertagna X., Jean C., Martinez A. Decreased expression of cyclic adenosine monophosphate-regulated aldose reductase (AKR1B1) is associated with malignancy in human sporadic adrenocortical tumors. J. Clin. Endocrinol. Metab. 2004, 89:3010-3019.
19. Looyenga B.D., Hammer G.D. Genetic removal of Smad3 from inhibin-null mice attenuates tumor progression by uncoupling extracellular mitogenic signals from the cell cycle machinery. Mol. Endocrinol. 2007, 21:2440-2457.
20. Massague J., Blain S.W., Lo R.S. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 2000, 103:295-309.
21. Matzuk M.M., Finegold M.J., Mather J.P., Krummen L., Lu H., Bradley A. Development of cancer cachexia-like syndrome and adrenal tumors in inhibin-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:8817-8821.
22. Nusse R. Wnt signaling in disease and in development. Cell Res. 2005, 15:28-32.
23. Parker K.L., Rice D.A., Lala D.S., Ikeda Y., Luo X., Wong M., Bakke M., Zhao L., Frigeri C., Hanley N.A., Stallings N., Schimmer B.P. Steroidogenic factor 1: an essential mediator of endocrine development. Recent Prog. Horm. Res. 2002, 57:19-36.
24. Pianovski M.A., Cavalli L.R., Figueiredo B.C., Santos S.C., Doghman M., Ribeiro R.C., Oliveira A.G., Michalkiewicz E., Rodrigues G.A., Zambetti G., Haddad B.R., Lalli E. SF-1 overexpression in childhood adrenocortical tumours. Eur. J. Cancer 2006, 42:1040-1043.
25. Roh J.S., Bondestam J., Mazerbourg S., Kaivo-Oja N., Groome N., Ritvos O., Hsueh A.J. Growth differentiation factor-9 stimulates inhibin production and activates Smad2 in cultured rat granulosa cells. Endocrinology 2003, 144:172-178.
26. Sasano H., Shizawa S., Suzuki T., Takayama K., Fukaya T., Morohashi K., Nagura H. Ad4BP in the human adrenal cortex and its disorders. J. Clin. Endocrinol. Metab. 1995, 80:2378-2380.
27. Sbiera S., Schmull S., Assie G., Voelker H.U., Kraus L., Beyer M., Ragazzon B., Beuschlein F., Willenberg H.S., Hahner S., Saeger W., Bertherat J., Allolio B., Fassnacht M. High diagnostic and prognostic value of steroidogenic factor-1 expression in adrenal tumors. J. Clin. Endocrinol. Metab. 2010, 95:E161-E171.
28. Suwa T., Chen M., Hawks C.L., Hornsby P.J. Zonal expression of dickkopf-3 and components of the Wnt signalling pathways in the human adrenal cortex. J. Endocrinol. 2003, 178:149-158.
29. Tissier F., Cavard C., Groussin L., Perlemoine K., Fumey G., Hagnere A.M., Rene-Corail F., Jullian E., Gicquel C., Bertagna X., Vacher-Lavenu M.C., Perret C., Bertherat J. Mutations of beta-catenin in adrenocortical tumors: activation of the Wnt signaling pathway is a frequent event in both benign and malignant adrenocortical tumors. Cancer Res. 2005, 65:7622-7627.
30. Tremblay J.J., Viger R.S. GATA factors differentially activate multiple gonadal promoters through conserved GATA regulatory elements. Endocrinology 2001, 142:977-986.
31. Vainio S., Heikkila M., Kispert A., Chin N., McMahon A.P. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999, 397:405-409.
32. Wajchenberg B.L., Albergaria Pereira M.A., Medonca B.B., Latronico A.C., Campos Carneiro P., Alves V.A., Zerbini M.C., Liberman B., Carlos Gomes G., Kirschner M.A. Adrenocortical carcinoma: clinical and laboratory observations. Cancer 2000, 88:711-736.
33. Weiss L.M. Comparative histologic study of 43 metastasizing and nonmetastasizing adrenocortical tumors. Am. J. Surg. Pathol. 1984, 8:163-169.
34. Weiss L.M., Medeiros L.J., Vickery A.L. Pathologic features of prognostic significance in adrenocortical carcinoma. Am. J. Surg. Pathol. 1989, 13:202-206.